Quantity-quality trade-off in the acquisition of token preference by capuchin monkeys (Sapajus spp.).

Money represents a cornerstone of human modern economies and how money emerged as a medium of exchange is a crucial question for social sciences. Although non-human primates have not developed monetary systems, they can estimate, combine and exchange tokens. Here, we evaluated quantity-quality trade-offs in token choices in tufted capuchin monkeys as a first step in the investigation of the generalizability of tokens as reinforcers, which is a potentially relevant factor underlying the emergence of money in humans. We measured capuchins' exchange preferences when they were repeatedly provided with 10 units of three token types yielding food combinations varying in quantity and quality. Overall, capuchins maximized their quantitative payoff, preferring tokens associated with a higher food amount, rather than showing violations of rationality. However, some individuals did not maximize their qualitative payoff, possibly because of conditional valuation effects or owing to the choice overload phenomenon, according to which too many options reduce the accuracy of choice. Our study supports the importance of comparative research to finely analyse the multiple components shaping the economic behaviours of other species, possibly to achieve a more comprehensive, evolutionary- and ecologically based understanding of human economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Social modulation of risky decision-making in rats (Rattus norvegicus) and tufted capuchin monkeys (Sapajus spp.).

Both human and non-human animals frequently deal with risky decisions in a social environment. Nevertheless, the influence of the social context on decision-making has been scarcely investigated. Here, we evaluated for the first time whether the presence of a conspecific influences risk preferences in rats and in tufted capuchin monkeys. Subjects received a series of choices between a constant, safe option and a variable, risky option, both alone (Alone condition) and when paired with a conspecific (Paired condition). The average payoff of the risky option was always lower than that of the safe option. Overall, the two species differed in their attitude towards risk: whereas rats were indifferent between options, capuchins exhibited a preference for the safe option. In both species, risk preferences changed in the Paired condition compared to the Alone condition, although in an opposite way. Whereas rats increased their risk preferences over time when paired with a conspecific, capuchins chose the risky option less in the Paired condition than in the Alone condition. Moreover, whereas anxiety-like behaviours decreased across sessions in rats, these behaviours where more represented in the Paired condition than in the Alone condition in capuchins. Thus, our findings extends to two distantly-related non-human species the evidence, so far available for human beings, that a decrease in anxiety corresponds to an increase in risk preferences, and vice versa. This suggests that the modulation of risk preferences by social influences observed in rats and capuchin monkeys may rely on a common, evolutionarily ancient, mechanism.

Delaying gratification for food and tokens in capuchin monkeys (Cebus apella) and chimpanzees (Pan troglodytes): when quantity is salient, symbolic stimuli do not improve performance.

Capuchin monkeys have been tested for the capacity to delay gratification for accumulating rewards in recent studies and have exhibited variable results. Meanwhile, chimpanzees have consistently excelled at this task. However, neither species have ever been tested at accumulating symbolic tokens instead of food items, even though previous reports indicate that tokens sometimes facilitate performance in other self-control tasks. Thus, in the present study, we tested capuchin monkeys and chimpanzees for their capacity to delay gratification in a delay maintenance task, in which an experimenter presented items, one at a time, to within reach of an animal for as long as the animal refrained from taking them. In Experiment 1, we assessed how long capuchin monkeys could accumulate items in the delay maintenance task when items were food rewards or tokens exchangeable for food rewards. Monkeys accumulated more food rewards than they did tokens. In Experiment 2, we tested capuchin monkeys and chimpanzees in a similar accumulation test. Whereas capuchins again accumulated more food than tokens, all chimpanzees but one showed no difference in performance in the two conditions. These findings provide additional evidence that chimpanzees exhibit greater self-control capacity in this task than do capuchin monkeys and indicate that symbolic stimuli fail to facilitate delay maintenance when they do not abstract away from the quantitative dimension of the task. This is consistent with previous findings on the effects of symbols on self-control and illuminates what makes accumulation a particularly challenging task.

Do capuchin monkeys (Cebus apella) use tokens as symbols?

In the absence of language, the comprehension of symbols is difficult to demonstrate. Tokens can be considered symbols since they arbitrarily stand for something else without having any iconic relation to their referent. We assessed whether capuchin monkeys (Cebus apella) can use tokens as symbols to represent and combine quantities. Our paradigm involved choices between various combinations of tokens A and B, worth one and three rewards, respectively. Pay-off maximization required the assessment of the value of each offer by (i) estimating token numerousness, (ii) representing what each token stands for and (iii) making simple computations. When one token B was presented against one to five tokens A (experiment 1), four out of ten capuchins relied on a flexible strategy that allowed to maximize their pay-off, i.e. they preferred one token B against one and two tokens A, and they preferred four or five tokens A against one token B. Moreover, when two tokens B were presented against three to six tokens A (experiment 2), two out of six capuchins performed summation over representation of quantities. These findings suggest that capuchins can use tokens as symbols to flexibly combine quantities.

The observation and hearing of eating actions activates motor programs related to eating in macaque monkeys.

The observation of actions can lead, in some cases, to the repetition of those same actions. In other words, motor programs similar to those observed can be recruited. Since this phenomenon is expressed when in the presence of another individual, it has been named social facilitation. In the present study we investigated whether the observation and/or hearing of eating actions facilitate eating behaviors in observing/listening pig-tailed macaques. In experiment 1, the observation of an eating room mate significantly enhanced eating behavior in the observer. Similar results were obtained (experiment 2) in response to the sound of eating actions but not to control sounds (experiment 3). We propose that eating facilitation triggered by observation or listening of eating actions can rely on the mirror neuron system of ventral premotor cortex that provides a matching between the observed/listened action and the executed action. This matching system can subsequently trigger the motor programs necessary for repeating the observed/heard actions.

Social facilitation of eating novel food in tufted capuchin monkeys (Cebus apella): input provided by group members and responses affected in the observer.

Learning about food palatability from watching what conspecifics eat might be one of the advantages of group living. A previous study investigated whether group members' presence or eating activity account for social facilitation of eating of foods never previously tasted. Capuchins encountered novel colored foods when (1) alone (Alone condition) or (2) with group members visible in the nearby cage (Group-present condition) or (3) with group members present and eating a familiar food that had not been colored (Group+food condition). Social facilitation of eating occurred when group members were eating, despite the difference in color between the familiar food eaten by them and the novel food presented to the experimental subject. To clarify what subjects learnt from group members when social facilitation occurred, we further analyze here the data from the previous study. The number of visual exposures to the colored novel food (as a group member) correlated with increased consumption of that novel food when encountered later (as experimental subject). In contrast, the number of times that an individual fed on the familiar food (as a group member) did not decrease its consumption of novel food (as experimental subject). Therefore, capuchins (1) habituated to the colors of the novel foods, and (2) did not take into account that seeing group members eating a food does not provide information about the palatability of a differently colored food. Since social facilitation of eating occurs when foods do not match in color, at least in capuchins, social facilitation of eating should not be considered as a way of learning about a safe diet, but rather as a way of overcoming neophobia.

Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys.

In primates, social context is one of the factors that increases the acceptance of novel foods. Previous experiments showed that tufted capuchins, Cebus apella, eat significantly more of novel foods when in the presence of group members eating the same novel foods. Several processes may have led to these results. The mere presence of group members may reduce the individual's stress of being alone, or its neophobic response and, consequently, may increase its food consumption. The individual may be influenced by what group members do, and local/stimulus enhancement and/or social facilitation may occur. To investigate the above processes, we assessed whether an individual capuchin monkey's consumption of novel foods is lower when (1) the individual is alone with nobody in the nearby cage than when (2) group members are present in the nearby cage with no food or when (3) they are present and eating a familiar food. We tested 15 subjects with three novel foods, each presented in one condition. In both social conditions, the more group members there were by the food box the more the experimental subject ate. In addition, when group members were present and eating food, there was a significant increase in the acceptance of the three foods, regardless of what group members were eating. We argue that social facilitation of eating is a quicker way to overcome neophobia and only social facilitation of eating what the others are eating can be considered a safe way to learn about a safe diet. Copyright 2000 The Association for the Study of Animal Behaviour.

Response to changes in food palatability in tufted capuchin monkeys, Cebus apella.

Palatability of plant foods may change over time in relation to the concentration of toxic secondary metabolites. We investigated the behavioural response of capuchin monkeys to this type of change and assessed the influence of social conditions. Twenty-seven tufted capuchin monkeys were presented in Social or Individual conditions with a familiar palatable food (phase 1), with the same familiar food to which pepper had been added, making it unpalatable (phase 2), and with the same familiar palatable food of phase 1 (phase 3). Five sessions were carried out in each phase. The capuchins adapted quickly to the change in food palatability by reducing (phase 2) and increasing (phase 3) the amounts of food eaten. The unpalatable food prompted an increase in olfactory exploration and in food processing. The experimental conditions (Social versus Individual) did not influence consumption, or any of the other behaviours. In addition, capuchins were more often near subjects with food in phases 2 and 3 in which palatability changed than in phase 1. These findings show that capuchins readily adjust to changes in flavour and palatability of a familiar food and that sudden unpalatability has no carry-over effects. Therefore, capuchins behave differently towards a familiar food whose palatability has changed than they do towards novel foods. Copyright 2000 The Association for the Study of Animal Behaviour.